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Pathogen-induced pH changes regulate the growth-defense balance in plants.

ABSTRACT: Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall-related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation-based proton pump activation in response to the fungus Fusarium oxysporum immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. In addition, pH seems to influence cellulose structure. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth-defense balance.

SUBMITTER: Kesten C

PROVIDER: S-EPMC6912046 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Pathogen-induced pH changes regulate the growth-defense balance in plants.

Kesten Christopher C Gámez-Arjona Francisco M FM Menna Alexandra A Scholl Stefan S Dora Susanne S Huerta Apolonio Ignacio AI Huang Hsin-Yao HY Tintor Nico N Kinoshita Toshinori T Rep Martijn M Krebs Melanie M Schumacher Karin K Sánchez-Rodríguez Clara C

The EMBO journal 20191118 24

Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall-related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplas ...[more]

PMID: 31736111

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Project description:The human fungal pathogen Candida albicans colonizes and infects various host sites with diverse environmental pH. Adaptation to these diverse pH conditions plays a crucial role in its success as a commensal and pathogen. The conserved Rim101 pH sensing pathway is responsible for neutral-alkaline pH responses in C. albicans. In this study, we identified a novel Rfg1-Bcr1 regulatory pathway that governs acidic pH responses and regulates filamentation in C. albicans. A null mutant library was screened, and we have identified Rfg1 and Bcr1 as key regulators of filamentation under acidic pH conditions. Rfg1 directly binds to the promoter region of Bcr1 to regulate its transcriptional expression, which in turn suppresses the filamentation of C. albicans. PHR1, an alkaline pH response gene, is significantly activated by the absence of Rfg1, indicating that Rfg1 regulates acidic pH response through the Rim101-Phr1 pathway. Moreover, the cAMP signaling pathway, transcription factors Efg1 and Flo8, and the hyphal-specific G1 cyclin Hgc1 play critical roles in the regulation. Our findings provide new insights into the mechanisms underlying the acidic pH response of C. albicans, which reflects its elaborate regulatory control of environmental adaptation.IMPORTANCECandida albicans is a human commensal and frequent pathogen that encounters a wide range of pH stresses. The ability of C. albicans to adapt to changes in extracellular pH is crucial for its success in colonization and pathogenesis. The Rim101 pH sensing pathway is well known to govern neutral-alkaline pH responses in this pathogen. Here, we report a novel Rfg1-Bcr1 regulatory pathway that governs acidic pH responses and regulates filamentous growth in C. albicans. In addition, the Rim101-Phr1 pathway, cAMP signaling pathway, transcription factors Efg1 and Flo8, and hyphal-specific G1 cyclin Hgc1 cooperate with this regulation. Our findings provide new insights into the regulatory mechanism of acidic pH response in C. albicans.

Dataset Information

Pathogen-induced pH changes regulate the growth-defense balance in plants.

Publications

Pathogen-induced pH changes regulate the growth-defense balance in plants.

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